Injury-stimulated Hedgehog signaling promotes regenerative proliferation of Drosophila intestinal stem cells

Journal of Cell Biology

Volumn 208, Issue 6, 2015, Pages 807-819

  Tian, Aiguo ^a   Shi, Qing ^a   Jiang, Alice ^a   Li, Shuangxi ^a   Wang, Bing ^a   Jiang, Jin ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; STRESS ACTIVATED PROTEIN KINASE; CELL SURFACE RECEPTOR; DROSOPHILA PROTEIN; HEDGEHOG PROTEIN, DROSOPHILA; PTC PROTEIN, DROSOPHILA;

ADULT; ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL PROLIFERATION; COMPARATIVE STUDY; DROSOPHILA; DROSOPHILA MELANOGASTER; IMMUNOHISTOCHEMISTRY; INTESTINAL STEM CELL; MIDGUT; MITOSIS INDEX; MUSCLE CELL; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ADULT STEM CELL; ANIMAL; CELL CULTURE; CYTOLOGY; FEMALE; GENETICS; INTESTINE; METABOLISM; PHYSIOLOGY; WOUND HEALING;

DROSOPHILA MELANOGASTER; ERINACEIDAE;

ADULT STEM CELLS; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; HEDGEHOG PROTEINS; INTESTINES; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; WOUND HEALING;

EID: 84925353057     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201409025     Document Type: Article

References (65)

1. Amcheslavsky, A., J. Jiang, and Y.T. Ip. 2009. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell. 4:49-61. http://dx.doi.org/10.1016/j.stem.2008.10.016.
2. Amcheslavsky, A., N. Ito, J. Jiang, and Y.T. Ip. 2011. Tuberous sclerosis complex and Myc coordinate the growth and division of Drosophila intestinal stem cells. J. Cell Biol. 193:695-710. http://dx.doi.org/10.1083/jcb.201103018.
3. Arimura, S., A. Matsunaga, T. Kitamura, K. Aoki, M. Aoki, and M.M. Taketo. 2009. Reduced level of Smoothened suppresses intestinal tumorigenesis by down-regulation of Wnt signaling. Gastroenterology. 137:629-638. http://dx.doi.org/10.1053/j.gastro.2009.04.059.
4. Bach, E.A., L.A. Ekas, A. Ayala-Camargo, M.S. Flaherty, H. Lee, N. Perrimon, and G.H. Baeg. 2007. GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr. Patterns. 7:323-331. http://dx.doi.org/10.1016/j.modgep.2006.08.003.
5. Beachy, P.A., S.S. Karhadkar, and D.M. Berman. 2004. Tissue repair and stem cell renewal in carcinogenesis. Nature. 432:324-331. http://dx.doi.org/10.1038/nature03100.
6. Berman, D.M., S.S. Karhadkar, A. Maitra, R. Montes De Oca, M.R. Gerstenblith, K. Briggs, A.R. Parker, Y. Shimada, J.R. Eshleman, D.N. Watkins, and P.A. Beachy. 2003. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature. 425:846-851. http://dx.doi.org/10.1038/nature01972.
7. Bielefeld, K.A., S. Amini-Nik, and B.A. Alman. 2013. Cutaneous wound healing: recruiting developmental pathways for regeneration. Cell. Mol. Life Sci. 70:2059-2081. http://dx.doi.org/10.1007/s00018-012-1152-9.
8. Biteau, B., and H. Jasper. 2011. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development. 138:1045-1055. http://dx.doi.org/10.1242/dev.056671.
9. Biteau, B., and H. Jasper. 2014. Slit/Robo signaling regulates cell fate decisions in the intestinal stem cell lineage of Drosophila. Cell Reports. 7:1867-1875. http://dx.doi.org/10.1016/j.celrep.2014.05.024.
10. Biteau, B., C.E. Hochmuth, and H. Jasper. 2011. Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. Cell Stem Cell. 9:402-411. http://dx.doi.org/10.1016/j.stem.2011.10.004.
11. Briscoe, J., and P.P. Thérond. 2013. The mechanisms of Hedgehog signalling and its roles in development and disease. Nat. Rev. Mol. Cell Biol. 14:416-429. http://dx.doi.org/10.1038/nrm3598.
12. Buchon, N., N.A. Broderick, S. Chakrabarti, and B. Lemaitre. 2009a. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 23:2333-2344. http://dx.doi.org/10.1101/gad.1827009.
13. Buchon, N., N.A. Broderick, M. Poidevin, S. Pradervand, and B. Lemaitre. 2009b. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe. 5:200-211. http://dx.doi.org/10.1016/j.chom.2009.01.003.
14. Buchon, N., D. Osman, F.P. David, H.Y. Fang, J.P. Boquete, B. Deplancke, and B. Lemaitre. 2013. Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Reports. 3:1725-1738. http://dx.doi.org/10.1016/j.celrep.2013.04.001.
15. Chen, Y., and G. Struhl. 1998. In vivo evidence that Patched and Smoothened constitute distinct binding and transducing components of a Hedgehog receptor complex. Development. 125:4943-4948.
16. Cordero, J.B., R.K. Stefanatos, A. Scopelliti, M. Vidal, and O.J. Sansom. 2012. Inducible progenitor-derived Wingless regulates adult midgut regeneration in Drosophila. EMBO J. 31:3901-3917. http://dx.doi.org/10.1038/emboj.2012.248.
17. Fendrich, V., F. Esni, M.V. Garay, G. Feldmann, N. Habbe, J.N. Jensen, Y. Dor, D. Stoffers, J. Jensen, S.D. Leach, and A. Maitra. 2008. Hedgehog signaling is required for effective regeneration of exocrine pancreas. Gastroenterology. 135:621-631: 631.e8. http://dx.doi.org/10.1053/j.gastro.2008.04.011.
18. Goulas, S., R. Conder, and J.A. Knoblich. 2012. The Par complex and integrins direct asymmetric cell division in adult intestinal stem cells. Cell Stem Cell. 11:529-540. http://dx.doi.org/10.1016/j.stem.2012.06.017.
19. Gu, D., Q. Fan, X. Zhang, and J. Xie. 2012. A role for transcription factor STAT3 signaling in oncogene Smoothened-driven carcinogenesis. J. Biol. Chem. 287:38356-38366. http://dx.doi.org/10.1074/jbc.M112.377382.
20. Guo, Z., I. Driver, and B. Ohlstein. 2013. Injury-induced BMP signaling negatively regulates Drosophila midgut homeostasis. J. Cell Biol. 201:945-961. http://dx.doi.org/10.1083/jcb.201302049.
21. Hsu, Y.C., L. Li, and E. Fuchs. 2014. Transit-amplifying cells orchestrate stem cell activity and tissue regeneration. Cell. 157:935-949. http://dx.doi.org/10.1016/j.cell.2014.02.057.
22. Jiang, H., and B.A. Edgar. 2009. EGFR signaling regulates the proliferation of Drosophila adult midgut progenitors. Development. 136:483-493. http://dx.doi.org/10.1242/dev.026955.
23. Jiang, H., and B.A. Edgar. 2012. Intestinal stem cell function in Drosophila and mice. Curr. Opin. Genet. Dev. 22:354-360. http://dx.doi.org/10.1016/j.gde.2012.04.002.
24. Jiang, H., P.H. Patel, A. Kohlmaier, M.O. Grenley, D.G. McEwen, and B.A. Edgar. 2009. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell. 137:1343-1355. http://dx.doi.org/10.1016/j.cell.2009.05.014.
25. Jiang, H., M.O. Grenley, M.J. Bravo, R.Z. Blumhagen, and B.A. Edgar. 2011. EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell. 8:84-95. http://dx.doi.org/10.1016/j.stem.2010.11.026.
26. Jiang, J., and C.C. Hui. 2008. Hedgehog signaling in development and cancer. Dev. Cell. 15:801-812. http://dx.doi.org/10.1016/j.devcel.2008.11.010.
27. Kapuria, S., J. Karpac, B. Biteau, D. Hwangbo, and H. Jasper. 2012. Notchmediated suppression of TSC2 expression regulates cell differentiation in the Drosophila intestinal stem cell lineage. PLoS Genet. 8:e1003045. http://dx.doi.org/10.1371/journal.pgen.1003045.
28. Karpowicz, P., J. Perez, and N. Perrimon. 2010. The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development. 137:4135-4145. http://dx.doi.org/10.1242/dev.060483.
29. Lee, T., and L. Luo. 2001. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24:251-254. http://dx.doi.org/10.1016/S0166-2236(00)01791-4.
30. Lee, W.C., K. Beebe, L. Sudmeier, and C.A. Micchelli. 2009. Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation. Development. 136:2255-2264. http://dx.doi.org/10.1242/dev.035196.
31. Li, Z., Y. Zhang, L. Han, L. Shi, and X. Lin. 2013. Trachea-derived Dpp controls adult midgut homeostasis in Drosophila. Dev. Cell. 24:133-143. http://dx.doi.org/10.1016/j.devcel.2012.12.010.
32. Li, Z., Y. Guo, L. Han, Y. Zhang, L. Shi, X. Huang, and X. Lin. 2014. Debramediated Ci degradation controls tissue homeostasis in Drosophila adult midgut. Stem Cell Rev. 2:135-144. http://dx.doi.org/10.1016/j.stemcr.2013.12.011.
33. Madison, B.B., K. Braunstein, E. Kuizon, K. Portman, X.T. Qiao, and D.L. Gumucio. 2005. Epithelial hedgehog signals pattern the intestinal cryptvillus axis. Development. 132:279-289. http://dx.doi.org/10.1242/dev.01576.
34. Marianes, A., and A.C. Spradling. 2013. Physiological and stem cell compartmentalization within the Drosophila midgut. eLife. 2:e00886. http://dx.doi.org/10.7554/eLife.00886.
35. Martín, V., G. Carrillo, C. Torroja, and I. Guerrero. 2001. The sterol-sensing domain of Patched protein seems to control Smoothened activity through Patched vesicular trafficking. Curr. Biol. 11:601-607. http://dx.doi.org/10.1016/S0960-9822(01)00178-6.
36. McGuire, S.E., Z. Mao, and R.L. Davis. 2004. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci. STKE. 2004:pl6.
37. Micchelli, C.A., and N. Perrimon. 2006. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature. 439:475-479. http://dx.doi.org/10.1038/nature04371.
38. Nakano, Y., I. Guerrero, A. Hidalgo, A. Taylor, J.R. Whittle, and P.W. Ingham. 1989. A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature. 341:508-513. http://dx.doi.org/10.1038/341508a0.
39. Ochoa, B., W.K. Syn, I. Delgado, G.F. Karaca, Y. Jung, J. Wang, A.M. Zubiaga, O. Fresnedo, A. Omenetti, M. Zdanowicz, et al. 2010. Hedgehog signaling is critical for normal liver regeneration after partial hepatectomy in mice. Hepatology. 51:1712-1723. http://dx.doi.org/10.1002/hep.23525.
40. Ohlstein, B., and A. Spradling. 2006. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature. 439:470-474. http://dx.doi.org/10.1038/nature04333.
41. Ohlstein, B., and A. Spradling. 2007. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science. 315:988-992. http://dx.doi.org/10.1126/science.1136606.
42. Peng, Y.C., C.M. Levine, S. Zahid, E.L. Wilson, and A.L. Joyner. 2013. Sonic hedgehog signals to multiple prostate stromal stem cells that replenish distinct stromal subtypes during regeneration. Proc. Natl. Acad. Sci. USA. 110:20611-20616. http://dx.doi.org/10.1073/pnas.1315729110.
43. Perdigoto, C.N., F. Schweisguth, and A.J. Bardin. 2011. Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine. Development. 138:4585-4595. http://dx.doi.org/10.1242/dev.065292.
44. Petrova, R., and A.L. Joyner. 2014. Roles for Hedgehog signaling in adult organ homeostasis and repair. Development. 141:3445-3457. http://dx.doi.org/10.1242/dev.083691.
45. Ramalho-Santos, M., D.A. Melton, and A.P. McMahon. 2000. Hedgehog signals regulate multiple aspects of gastrointestinal development. Development. 127:2763-2772.
46. Ren, F., B. Wang, T. Yue, E.Y. Yun, Y.T. Ip, and J. Jiang. 2010. Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc. Natl. Acad. Sci. USA. 107:21064-21069. http://dx.doi.org/10.1073/pnas.1012759107.
47. Ren, F., Q. Shi, Y. Chen, A. Jiang, Y.T. Ip, H. Jiang, and J. Jiang. 2013. Drosophila Myc integrates multiple signaling pathways to regulate intestinal stem cell proliferation during midgut regeneration. Cell Res. 23:1133-1146. http://dx.doi.org/10.1038/cr.2013.101.
48. Scopelliti, A., J.B. Cordero, F. Diao, K. Strathdee, B.H. White, O.J. Sansom, and M. Vidal. 2014. Local control of intestinal stem cell homeostasis by enteroendocrine cells in the adult Drosophila midgut. Curr. Biol. 24:1199-1211. http://dx.doi.org/10.1016/j.cub.2014.04.007.
49. Shaw, R.L., A. Kohlmaier, C. Polesello, C. Veelken, B.A. Edgar, and N. Tapon. 2010. The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development. 137:4147-4158. http://dx.doi.org/10.1242/dev.052506.
50. Shin, K., J. Lee, N. Guo, J. Kim, A. Lim, L. Qu, I.U. Mysorekar, and P.A. Beachy. 2011. Hedgehog/Wnt feedback supports regenerative proliferation of epithelial stem cells in bladder. Nature. 472:110-114. http://dx.doi.org/10.1038/nature09851.
51. Singh, S., Z. Wang, D. Liang Fei, K.E. Black, J.A. Goetz, R. Tokhunts, C. Giambelli, J. Rodriguez-Blanco, J. Long, E. Lee, et al. 2011. Hedgehogproducing cancer cells respond to and require autocrine Hedgehog activity. Cancer Res. 71:4454-4463. http://dx.doi.org/10.1158/0008-5472. CAN-10-2313.
52. Sisson, J.C., K.S. Ho, K. Suyama, and M.P. Scott. 1997. Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell. 90:235-245. http://dx.doi.org/10.1016/S0092-8674(00)80332-3.
53. Staley, B.K., and K.D. Irvine. 2010. Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr. Biol. 20:1580-1587. http://dx.doi.org/10.1016/j.cub.2010.07.041.
54. Taipale, J., and P.A. Beachy. 2001. The Hedgehog and Wnt signalling pathways in cancer. Nature. 411:349-354. http://dx.doi.org/10.1038/35077219.
55. Tian, A., and J. Jiang. 2014. Intestinal epithelium-derived BMP controls stem cell self-renewal in Drosophila adult midgut. eLife. 3:e01857. http://dx.doi.org/10.7554/eLife.01857.
56. van den Brink, G.R., S.A. Bleuming, J.C. Hardwick, B.L. Schepman, G.J. Offerhaus, J.J. Keller, C. Nielsen, W. Gaffield, S.J. van Deventer, D.J. Roberts, and M.P. Peppelenbosch. 2004. Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat. Genet. 36:277-282. http://dx.doi.org/10.1038/ng1304.
57. Varnat, F., A. Duquet, M. Malerba, M. Zbinden, C. Mas, P. Gervaz, and A. Ruiz i Altaba. 2009. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol. Med. 1:338-351. http://dx.doi.org/10.1002/emmm.200900039.
58. Varnat, F., G. Zacchetti, and A. Ruiz i Altaba. 2010. Hedgehog pathway activity is required for the lethality and intestinal phenotypes of mice with hyperactive Wnt signaling. Mech. Dev. 127:73-81. http://dx.doi.org/10.1016/j.mod.2009.10.005.
59. Wang, G., K. Amanai, B. Wang, and J. Jiang. 2000. Interactions with Costal2 and Suppressor of fused regulate nuclear translocation and activity of Cubitus interruptus. Genes Dev. 14:2893-2905. http://dx.doi.org/10.1101/gad.843900.
60. Weston, C.R., and R.J. Davis. 2007. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19:142-149. http://dx.doi.org/10.1016/j.ceb.2007.02.001.
61. Xu, N., S.Q. Wang, D. Tan, Y. Gao, G. Lin, and R. Xi. 2011. EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. Dev. Biol. 354:31-43. http://dx.doi.org/10.1016/j.ydbio.2011.03.018.
62. Yauch, R.L., S.E. Gould, S.J. Scales, T. Tang, H. Tian, C.P. Ahn, D. Marshall, L. Fu, T. Januario, D. Kallop, et al. 2008. A paracrine requirement for hedgehog signalling in cancer. Nature. 455:406-410. http://dx.doi.org/10.1038/nature07275.
63. Zeng, X., C. Chauhan, and S.X. Hou. 2010. Characterization of midgut stem cell-and enteroblast-specific Gal4 lines in drosophila. Genesis. 48:607-611. http://dx.doi.org/10.1002/dvg.20661.
64. Zhang, W., Y. Zhao, C. Tong, G. Wang, B. Wang, J. Jia, and J. Jiang. 2005. Hedgehog-regulated Costal2-kinase complexes control phosphorylation and proteolytic processing of Cubitus interruptus. Dev. Cell. 8:267-278. http://dx.doi.org/10.1016/j.devcel.2005.01.001.
65. Zhou, F., A. Rasmussen, S. Lee, and H. Agaisse. 2013. The UPD3 cytokine couples environmental challenge and intestinal stem cell division through modulation of JAK/STAT signaling in the stem cell microenvironment. Dev. Biol. 373:383-393. http://dx.doi.org/10.1016/j.ydbio.2012.10.023.